5 Gibberellins in Fungi, Bacteria and Lower Plants: Biosynthesis, Function and Evolution
Bettina Tudzynski
Westfälische Wilhelms-Universität Münster, Institut für Biologie und Biotechnologie der Pflanzen, Germany
Search for more papers by this authorLena Studt
Westfälische Wilhelms-Universität Münster, Institut für Biologie und Biotechnologie der Pflanzen, Germany
Search for more papers by this authorMaría Cecilia Rojas
Laboratorio de Bioorgánica, Departamento de Química, Facultad de Ciencias, Universidad de Chile, Chile
Search for more papers by this authorBettina Tudzynski
Westfälische Wilhelms-Universität Münster, Institut für Biologie und Biotechnologie der Pflanzen, Germany
Search for more papers by this authorLena Studt
Westfälische Wilhelms-Universität Münster, Institut für Biologie und Biotechnologie der Pflanzen, Germany
Search for more papers by this authorMaría Cecilia Rojas
Laboratorio de Bioorgánica, Departamento de Química, Facultad de Ciencias, Universidad de Chile, Chile
Search for more papers by this authorAbstract
The rice pathogen Fusarium fujikuroi, as well as two distantly related fungi, Sphaceloma manihoticola and Phaeosphaeriae sp., contains clusters of gibberellin (GA) biosynthesis genes and produces GAs. Fungal GAs are structurally identical to those synthesised by higher plants, although the respective biosynthetic pathways, genes and enzymes differ. Besides fungi, some bacteria synthesise GAs. An operon of GA biosynthesis genes was found in the symbiotic rhizobacterium Bradyrhizobium japonicum and in other Rhizobium species. This operon encodes the enzymes of GA9 biosynthesis and includes a reductase or alcohol dehydrogenase gene not present in fungal clusters. Differences between genes and enzymes indicate convergent evolution of the GA biosynthesis pathway in higher plants, fungi and bacteria. In contrast to higher plants, GAs are not produced by all lower plants. Mosses or liverworts synthesise ent-kaurenoids, but not GAs, while lycophytes and ferns synthesise GAs or GA-related products that participate in the regulation of reproductive development.
References
- Abul, Y., Menéndez, V., Gómez-Campo, C. et al. (2010). Occurrence of plant growth regulators in Psilotum nudum . Journal of Plant Physiology 167, 1211–1213.
- Albermann, S., Linnemannstöns, P. and Tudzynski, B. (2013a). Strategies for strain improvement in Fusarium fujikuroi: overexpression and localization of key enzymes of the isoprenoid pathway and their impact on gibberellin biosynthesis. Applied Microbiology and Biotechnology 97, 2979–2995.
- Albermann, S., Elter, T., Teubner, A. et al. (2013b). Characterization of novel mutants with an altered gibberellin spectrum in comparison to different wild-type strains of Fusarium fujikuroi . Applied Microbiology and Biotechnology 97, 7779–7790.
- Anterola, A. and Shanle, E.K. (2008). Genomic insights in moss gibberellin biosynthesis. Bryologist 111, 218–230.
- Anterola, A., Shanle, E.K., Mansouri, K. et al. (2009). Gibberellin precursor is involved in spore germination in the moss Physcomitrella patens . Planta 229, 1003–1007.
- Atzorn, R., Crozier, A., Wheeler, C. and Sandberg, G. (1988). Production of gibberellins and indole 3-acetic acid by Rhizobium phaseoli in relation to nodulation of Phaseolus vulgaris roots. Planta 175, 532–538.
- Aya, K., Hiwatashi, Y., Kojima, M. et al. (2011). The gibberellin perception system evolved to regulate a pre-existing GAMYB-mediated system during land plant evolution. Nature Communications 2, 544.
- Bastian, F., Cohen, A., Piccoli, P. et al. (1998). Production of indole-3-acetic acid and gibberellins A1 and A3 by Acetobacter diazotrophicus and Herbaspirillum seropedicae in chemically-defined culture media. Plant Growth Regulation 24, 7–11.
- Bearder, J.R. (1983). In vivo diterpenoid biosynthesis in Gibberella fujikuroi: the pathway after ent-kaurene. In The Biochemistry and Physiology of Gibberellins (ed. A. Crozier), Praeger Publishers, New York, pp. 251–387.
- Bhattacharya, A., Kourmpetli, S., Ward, D.A. et al. (2012). Characterization of the fungal gibberellin desaturase as a 2-oxoglutarate-dependent dioxygenase and its utilization for enhancing plant growth. Plant Physiology 160, 837–845.
- Bömke, C. and Tudzynski, B. (2009). Diversity, regulation and evolution of the gibberellin biosynthetic pathway in fungi compared to plants and bacteria. Phytochemistry 70, 1876–1893.
- Bömke, C., Rojas, M.C., Gong, F. et al. (2008a). Isolation and characterization of the gibberellin biosynthetic gene cluster in Sphaceloma manihoticola . Applied and Environmental Microbiology 74, 5325–5339.
- Bömke, C., Rojas, M.C., Hedden, P. and Tudzynski, B. (2008b). Loss of gibberellin production is due to a deletion in the gibberellic acid gene cluster in Fusarium verticillioides (G. Fujikuroi MP-A) Applied and Environmental Microbiology 74, 7790–7801.
- Bottini, R., Fulchieri, M., Pearce, D. and Pharis, R.P. (1989). Identification of gibberellins A1, A3, and isoA3 in cultures of Azospirillum lipoferum . Plant Physiology 90, 45–47.
- Bottini, R., Cassán, F. and Piccoli, P. (2004). Gibberellin production by bacteria and its involvement in plant growth promotion and yield increase. Applied Microbiology and Biotechnology 65, 497–503.
- Cassán, F., Lucangeli, C.D., Bottini, R. and Piccoli, P. (2001a). Azospirillum spp. metabolize [17,17-2H2 ]gibberellin A20 to [17,17-2H2 ]gibberellin A1 in vivo dy rice mutant seedlings. Plant Cell Physiology 42, 763–767.
- Cassán, F., Bottini, R., Schneider, G. and Piccoli, P. (2001b). Azospirillum brasilense and Azospirillum lipoferum hydrolyze conjugates of GA20 and metabolize the resultant aglicones to GA1 in seedlings of rice dwarf mutants. Plant Physiology 125, 2053–2058.
- Chapman, M.A. and Regan M.A. (1980). Evolution of a biochemical pathway: evidence from comparative biochemistry. Annual Review of Plant Physiology 31, 639–645.
- Dean, R.A., Talbot, N.J., Ebbole, D.J. et al. (2005). The genome sequence of the rice blast fungus Magnaporthe grisea . Nature 434, 980–986.
- DeBose-Boyd, R.A. (2008). Feedback regulation of cholesterol synthesis: sterol-accelerated ubiquitination and degradation of HMG CoA reductase. Cell Research 18, 609–621.
- Ergün, N., Topcuoglu, S.F. and Yildiz, A. (2002). Auxin (indole-3-acetic acid), gibberellic acid (GA3), abscisic acid (ABA) and cytokinin (zeatin) production by some species of mosses and lichens. Turkish Journal of Botany 26, 13–18.
- Fourie, G., van der Merwe, N.A., Wingfield, B.D. et al. (2013). Evidence for inter-specific recombination among the mitochondrial genomes of Fusarium species in the Gibberella fujikuroi complex. BMC Genomics 14, 605–619.
- Freiberg, C., Fellay, R., Bairoch, A. et al. (1997). Molecular basis of symbiosis between Rhizobium and legumes. Nature 387, 394–401.
- Gutierrez-Mañero, F., Ramos-Solano, B., Probanza, A. et al. (2001). The plant growth-promoting rhizobacteria Bacillus pumilus and Bacillus licheniformis produce high amounts of physiologically active gibberellins. Physiologia Plantarum 111, 206–211.
- Hartweck, L.M. (2008). Gibberellin signaling. Planta 229, 1–13.
- Hauser, F., Pessi, G., Friberg, M. et al. (2007). Dissection of the Bradyrhizobium japonicum NifA+σ54 regulon, and identification of a ferredoxin gene (fdxN) for symbiotic nitrogen fixation. Molecular Genetics and Genomics 278, 255–271.
- Hayashi, K., Kawaide, H., Notomi, et al. (2006). Identification and functional analysis of bifunctional ent-kaurene synthase from the moss Physcomitrella patens . FEBS Letters 580, 6175–6181.
- Hayashi, K., Horie, K., Hiwatashi, Y. et al. (2010). Endogenous diterpenes derived from ent-kaurene, a common gibberellin precursor, regulate protonema differentiation of the moss Physcomitrella patens . Plant Physiology 153, 1085–1097.
- Hedden, P. and Kamiya, Y. (1997). Gibberellin biosynthesis: enzymes, genes and their regulation. Annual Review of Plant Physiology and Plant Molecular Biology 48, 431–460.
- Hedden, P. and Phillips, A.L. (2000). Manipulation of hormone biosynthetic genes in transgenic plants. Current Opinion in Biotechnology 11, 130–137.
- Hedden, P. and Thomas, S.G. (2012). Gibberellin biosynthesis and its regulation. Biochemical Journal 444, 11–25.
- Hedden, P., MacMillan, J. and Phinney, B.O. (1974). Fungal products. Part XII. Gibberellin A14-aldehyde, an intermediate in gibberellin biosynthesis in Gibberella fujikuroi. Journal of the Chemical Society , Perkin Transactions 1, 587–592.
- Hedden, P., Phillips, A.L., Rojas, M.C., et al. (2002). Gibberellin biosynthesis in plants and fungi: a case of convergent evolution? Journal of Plant Growth Regulation 20, 319–331.
- Hershey, D.M., Lu, X., Zi, J. and Peters, R.J. (2014). Functional conservation of the capacity for ent-kaurene biosynthesis and an associated operon in certain rhizobia. Journal of Bacteriology 196, 100–106.
- Hirano, K., Nakajima, M., Asano, K. et al. (2007). The GID1-mediated gibberellin perception mechanism is conserved in the lycophyte Selaginella moellendorffii but not in the bryophyte Physcomitrella patens . The Plant Cell 19, 3058–3079.
- Hirano, K., Ueguchi-Tanaka, M. and Matsuoka, M. (2008). GID1-mediated gibberellin signaling in plants. Trends in Plant Science 13, 192–199.
- Homann, V., Mende, K., Arntz, C. et al. (1996). The isoprenoid pathway: cloning and characterization of fungal FPPS genes. Current Genetics 30, 232–239.
- Hori, S. (1898). Some observations on ‘Bakanae’ disease of the rice plant. Memoirs of Agricultural Research (Tokyo) 12, 110–119.
- Hou, X., Lee, L.Y., Xia, K. et al. (2010). DELLAs modulate jasmonate signaling via competitive binding to JAZs. Developmental Cell 19, 884–894.
- Janzen, R., Rood, S., Dormar, J. and McGill, W. (1992). Azospirillum brasilense produces gibberellins in pure cultures, chemically-defined medium and in co-culture on straw. Soil Biology and Biochemistry 24, 1061–1064.
- Kang, S-M., Khan, A.L., Hamayun, M. et al. (2012). Gibberellin-producing Promicromonospora sp. SE188 improves Solanum lycopersicum plant growth and influences endogenous plant hormones. Journal of Microbiology 50, 902–909.
- Kang, S-M., Khan, A.L., You, Y-H., et al. (2013). Gibberellin production by newly isolated strain of Leifsonia soli SE134 and its potential for plant growth promotion. Journal of Microbiology and Biotechnology 24, 106–112.
- Kawaide, H., Sassa, T. and Kamiya, Y. (1995). Plant-like biosynthesis of gibberellin A1 in the fungus Phaeosphaeria sp. L487. Phytochemistry 39, 305–310.
- Kawaide, H., Imai, R., Sassa, T. and Kamiya, Y. (1997). ent-Kaurene synthase from the fungus Phaeosphaeria sp. L487: cDNA isolation, characterization, and bacterial expression of a bifunctional diterpene cyclase in fungal gibberellin biosynthesis. Journal of Biological Chemistry 272, 21706–21712.
- Kawaide, H. (2006). Biochemical and molecular analyses of gibberellin biosynthesis in fungi. Bioscience, Biotechnology, and Biochemistry 70, 583–590.
- Kawaide, H., Hayashi, K., Kawanabe, R. et al. (2011). Identification of the single amino acid involved in quenching the ent-kauranyl cation by a water molecule in ent-kaurene synthase of Physcomitrella patens . FEBS Journal 278, 123–133.
- Keister, D.L., Tully, R.E. and van Berkum, P. (1999). A cytochrome P450 gene cluster in the Rhizobiaceae . The Journal of General and Applied Microbiology 45, 301–303.
- Kurumatani, M., Yagi, K., Murata, T. et al. (2001). Isolation and identification of antheridiogens in the ferns Lygodium microphyllum and Lygodium reticulatum . Bioscience Biotechnology and Biochemistry 65, 2311–2314.
- Lange, T., Hedden, P. and Graebe, J.E. (1994). Expression cloning of a gibberellin 20-oxidase, a multifunctional enzyme involved in gibberellin biosynthesis. Proceedings of the National Academy of Sciences USA 91, 8552–8556.
- Linnemannstöns, P., Voß, T., Hedden, P. et al. (1999). Deletions in the gibberellin biosynthesis gene cluster of Gibberella fujikuroi by restriction enzyme-mediated mutagenesis. Applied and Environmental Microbiology 65, 2558–2564.
- Liu, W., Feng, X., Zheng, Y. et al., (2014). Structure, function and inhibition of ent-kaurene synthase from Bradyrhizobium japonicum . Scientific Reports 4, 6214.
- Lucangeli, C. and Bottini, R. (1996). Reversion of dwarfism in dwarf-1 maize (Zea mays L.) and dwarf-x rice (Oryza sativa L.) mutants by endophytic Azospirillum spp . Biocell 20, 223–228.
- Lucangeli, C. and Bottini, R. (1997). Effects of Azospirillum spp. on endogenous gibberellins content and growth of maize (Zea mays L.) treated with uniconazole. Symbiosis 23, 63–72.
- MacMillan, J. (1997). Biosynthesis of the gibberellin plant hormones. Natural Product Reports 14, 221–243.
- MacMillan, J. (2002). Occurrence of gibberellins in vascular plants, fungi and bacteria. Journal of Plant Growth Regulation 20, 387–442.
- Malonek, S., Bömke, C., Bornberg-Bauer, E. et al. (2005a). Distribution of gibberellin biosynthetic genes and gibberellin production in the Gibberella fujikuroi species complex. Phytochemistry 66, 1296–1311.
- Malonek, S., Rojas, M.C., Hedden, P., et al., (2005b). Functional characterization of two cytochrome P450 monooxygenase genes, P450–1 and P450–4, of the gibberellic acid gene cluster in Fusarium proliferatum (Gibberella fujikuroi MP-D). Applied and Environmental Microbiology 71, 1462–1472.
- Malonek, S., Rojas, M.C., Hedden, P., et al., (2005c). Restoration of gibberellin production in Fusarium proliferatum by functional complementation of enzymatic blocks. Applied and Environmental Microbiology 71, 6014–6025.
- Mende, K., Homann, V. and Tudzynski, B. (1997). Molecular characterization of the geranylgeranyl diphosphate synthase gene of Gibberella fujikuroi . Molecular and General Genetics 255, 96–105.
- Méndez, C., Baginsky, C., Hedden, P. et al. (2014). Gibberellin oxidase activities in Bradyrhizobium japonicum bacteroids. Phytochemistry 98, 101–109.
- Menéndez, V., Revilla, M.A., Bernard, P., et al. (2006a). Gibberellins and antheridiogen on sex in Blechnum spicant L. Plant Cell Reports 25, 1104–1110.
- Menéndez, V., Villacorta, N.F., Revilla, M.A., et al. (2006b). Exogenous and endogenous growth regulators on apogamy in Dryopteris affinis (Lowe) Fraser-Jenkins sp. affinis . Plant Cell Reports 25, 85–91.
- Miyazaki, S., Katsumata, T., Natsume, M. and Kawaide, H. (2011). The CYP701B1 of Physcomitrella patens is an ent-kaurene oxidase that resists inhibition by uniconazole-P. FEBS Letters 585, 1879–1883.
- Morrone, D., Chambers, J., Lowry, L. et al. (2009). Gibberellin biosynthesis in bacteria: separate ent-copalyl diphosphate and ent-kaurene synthases in Bradyrhizobium japonicum . FEBS Letters 583, 475–480.
- Mowat, J.A. (1965). A survey of results on the occurrence of auxins and gibberellins in algae. Botanica Marina 8, 149–155.
- Nagashima, F., Kasai, W., Kondoh, M., et al. (2003). New ent-kaurene-type diterpenoids possessing cytotoxicity from the New Zealand liverwort Jungermannia species. Chemical and Pharmaceutical Bulletin 51, 1189–1192.
- Navarro, L, Bari, R., Achard, P. et al. (2008). DELLAs control plant immune responses by modulating the balance of jasmonic acid and salicylic acid signaling. Current Biology 18, 650–655.
- Nozaki, H., Hayashi, K., Okuda, K., et al. (2007). ent-Kaurene-type diterpenoids from a suspension culture of the liverwort Jungermannia subulata . Planta Medica 73, 689–695.
- Pessi, G., Ahrens, C.H., Rehrauer, H. et al. (2007). Genome-wide transcript analysis of Bradyrhizobium japonicum bacteroids in soybean root nodules. Molecular Plant–Microbe Interactions 20, 1353–1363.
- Phillips, A.L., Ward, D.A., Uknes, S. et al. (1995). Isolation and expression of three gibberellin 20-oxidase cDNA clones from Arabidopsis . Plant Physiology 108, 1049–1057.
- Piccoli, P. and Bottini, R. (1994). Metabolism of 17,17-[2H]gibberellin A20 to 17,17-[2H]gibberellin A1 by Azospirillum lipoferum cultures. AgriScientia 9, 13–15.
- Piccoli, P., Masciarelli, O. and Bottini, R. (1996). Metabolism of 17,17[2H2]-gibberellins A4, A9 and A20 by Azospirillum lipoferum in chemically-defined culture medium. Symbiosis 21, 263–274.
- Piccoli, P., Lucangelli, D., Schneider, G. and Bottini, R. (1997). Hydrolysis of [17, 17-2H2] gibberellin A20-glucosyl ester by Azospirillum lipoferum cultured in a nitrogen-free biotin-based chemically-defined medium. Plant Growth Regulation 23, 179–182.
- Piccoli, P., Travaglia, C., Cohen, A. et al. (2011). An endophytic bacterium isolated from roots of the halophyte Prosopis strombulifera produces ABA, IAA, gibberellins A1 and A3 and jasmonic acid in chemically-defined culture medium. Plant Growth Regulation 64, 207–210.
- Rademacher, W. and Graebe, J.E. (1979). Gibberellin A4 produced by Sphaceloma manihoticola, the cause of the superelongation disease of cassava (Manihot esculenta). Biochemical and Biophysical Research Communications 91, 35–40.
- Radley, M. (1956). Occurrence of substances similar to gibberellic acid in higher plants. Nature 178, 1070–1071.
- Rensing, S.A., Lang, D., Zimmer, A.D. et al. (2008). The Physcomitrella patens genome reveals evolutionary insights into the conquest of land by plants. Science 319, 64–69.
- Rim, S.-O., Lee, J.-H., Choi, W.-Y., et al. (2005). Fusarium proliferatum KGL0401 as a new gibberellin-producing fungus. Journal of Microbiology and Biotechnology 15, 809–814.
- Rojas, M.C., Hedden, P., Gaskin, P. and Tudzynski, B. (2001). The P450-1 gene of Gibberella fujikuroi encodes a multifunctional enzyme in gibberellin biosynthesis. Proceedings of the National Academy of Sciences USA 98, 5838–5843.
- Salazar, E., Díaz-Mejía, J., Moreno-Hagelsieb, G. et al. (2010). Characterization of the NifA-RpoN Regulon in Rhizobium etli in free life and in symbiosis with Phaseolus vulgaris . Applied and Environmental Microbiology 76, 4510–4520.
- Sassa, T. and Suzuki, K. (1990). Metabolism of gibberellin A9 to gibberellin A4 in a new gibberellin-producing fungus, Phaeosphaeria sp. L487. Agricultural and Biological Chemistry 54, 3373–3375.
- Sassa, T., Suzuki, K. and Haruki, E. (1989). Isolation and identification of gibberellins A4 and A9 from a fungus Phaeosphaeria sp. Agricultural and Biological Chemistry 53, 303–304.
- Sawada, K. (1912). Diseases of agricultural products in Japan. Formosan Agricultural Reviews 63, 10–16.
- Schardl, C.L., Young, C.A., Hesse, U., et al. (2012). Plant-symbiotic fungi as chemical engineers: multi-genome analysis of the Clavicipitaceae reveals dynamics of alkaloid loci. PLoS Genetics 9, e1003323.
- Sponsel, V.M. and Hedden, P. (2004). Gibberellin biosynthesis and inactivation. In Plant Hormones. Biosynthesis, Signal transduction , Action! (ed. P.J. Davies.), Kluwer Academic Publishers, Dordrecht, the Netherlands, pp. 63–94.
- Sun, T-P. (2011) The molecular mechanism and evolution of the GA-GID1-DELLA signaling module in plants. Current Biology 21, R338-R345.
- Sun, T.-P. and Kamiya, Y. (1994). The Arabidopsis GA1 locus encodes the cyclase ent-kaurene synthase A of gibberellin biosynthesis. The Plant Cell 6, 1509–1518.
- Tanaka, J., Yano, K., Aya, K., et al. (2014). Antheridiogen determines sex in ferns via spatiotemporally split gibberellin synthesis pathway. Science 346, 469–473.
- Toyomasu, T., Nakaminami, K., Toshima, H. et al. (2004). Cloning of a gene cluster responsible for the biosynthesis of diterpene aphidicolin, a specific inhibitor of DNA polymerase α. Bioscience, Biotechnology, and Biochemistry 68, 146–152.
- Troncoso, C., González, X., Bömke, C. et al. (2010). Gibberellin biosynthesis and gibberellin oxidase activities in Fusarium sacchari, Fusarium konzum and Fusarium subglutinans strains. Phytochemistry 71, 1322–1331.
- Tsavkelova, E.A., Bömke, C., Netrusov, A.I., et al. (2008). Production of gibberellic acids by an orchid-associated Fusarium proliferatum strain. Fungal Genetics and Biology 45, 1393–1403.
- Tudzynski, B. (2005). Gibberellin biosynthesis in fungi: genes, enzymes and impact on biotechnology. Applied Microbiology and Biotechnology 66, 597–611.
- Tudzynski, B. and Hölter, K. (1998). Gibberellin biosynthetic pathway in Gibberella fujikuroi: evidence for a gene cluster. Fungal Genetics and Biology 25, 157–170.
- Tudzynski, B., Kawaide, H. and Kamiya, Y. (1998). Gibberellin biosynthesis in Gibberella fujikuroi: cloning and characterization of the copalyl diphosphate synthase gene. Current Genetics 34, 234–240.
- Tudzynski, B., Hedden, P., Carrera, E. and Gaskin P. (2001). The P450-4 gene of Gibberella fujikuroi encodes ent-kaurene oxidase in the gibberellin biosynthesis pathway. Applied and Environmental Microbiology 67, 3514–3522.
- Tudzynski, B., Rojas, M.C., Gaskin, P. and Hedden, P. (2002). The gibberellin 20-oxidase of Gibberella fujikuroi is a multifunctional monooxygenase. Journal of Biological Chemistry 277, 21246–21253.
- Tudzynski, B., Mihlan, M., Rojas, M.C., et al. (2003). Characterization of the final two genes of the gibberellin biosynthesis gene cluster of Gibberella fujikuroi: des and P450-3 encode GA4 desaturase and the 13-hydroxylase, respectively. Journal of Biological Chemistry 278, 28635–28643.
- Tully, R.E. and Keister, D.L. (1993). Cloning and mutagenesis of a cytochrome P-450 locus from Bradyrhizobium japonicum that is expressed anaerobically and symbiotically. Applied and Environmental Microbiology 59, 4136–4142.
- Tully, R.E., van Berkum, P., Lovins, et al. (1998). Identification and sequencing of a cytochrome P450 gene cluster from Bradyrhizobium japonicum . Biochimica et Biophysica Acta 1398, 243–255.
- Urrutia, O., Hedden, P., Rojas, M.C., et al. (2001). Monooxygenases involved in GA12 and GA14 synthesis in Gibberella fujikuroi . Phytochemistry 56, 5005–5011.
- Vandenbussche, F., Fierro, A.C., Wiedemann, G., et al. (2007). Evolutionary conservation of plant gibberellin signalling pathway components. BMC Plant Biology 7, 1–17.
- von Schwartzenberg, K., Schulte, W. and Kassner, H. (2004). The moss Physcomitrella patens releases a tetracyclic diterpene. Plant Cell Reports 22, 780–786.
- Wiemann, P., Albermann, S., Niehaus, E. et al. (2012). The Sfp-type 4'-phosphopantetheinyl transferase Ppt1 of Fusarium fujikuroi controls development, secondary metabolism and pathogenicity. PLoS One 7, e37519.
- Wiemann, P., Sieber, C.M.-K., von Bargen, K.W. et al. (2013). Deciphering the cryptic genome: genome-wide analyses of the rice pathogen Fusarium fujikuroi reveal complex regulation of secondary metabolism and novel metabolites. PLoS Pathogens 9, e1003475.
- Wingfield, B.D., Steenkamp. E.T., Santana Q. et al. (2012). First fungal genome sequence from Africa: Consequences scientific and regional. South African Journal of Science 108, 1–9.
- Woitek, S., Unkles, S.E., Kinghorn, J.R. and Tudzynski, B. (1997). 3-Hydroxy-3-methylglutaryl-CoA reductase gene of Gibberella fujikuroi: isolation and characterization. Current Genetics 31, 38–47.
-
Yabuta, T. and Sumiki, Y. (1938). On the crystal of gibberellin, a substance to promote plant growth. Journal of the Agricultural Chemical Society of Japan
14, 1526.
10.1271/nogeikagaku1924.14.12_1526 Google Scholar
- Yamane, H., Fujioka, S., Spray, C.R. et al. (1988). Endogenous gibberellins from sporophytes of two tree ferns, Cibotium glaucum and Dicksonia antarctica . Plant Physiology 86, 857–862.
- Yamauchi, T., Oyama, N., Yamane, H. et al. (1996). Identification of antheridiogens in Lygodium circinnatum and Lygodium flexuosum . Plant Physiology 111, 741–745.
- Yamaguchi, S. (2008). Gibberellin metabolism and its regulation. Annual Review of Plant Biology 59, 225–251.
- Yasumura, Y., Crumpton-Taylor, M., Fuentes, S. and Harberd, N.P. (2007). Step-by-step acquisition of the gibberellin-DELLA growth-regulatory mechanism during land-plant evolution. Current Biology 17, 1225–1230.
- Zhang, S., Monahan, B.J., Tkacz, J.S. and Scott, B. (2004). Indole-diterpene gene cluster from Aspergillus flavus . Applied and Environmental Microbiology 70, 6875–6883.
- Zeigler, R.S., Powell, L.E. and Thurston, H.D. (1980). Gibberellin A4 production by Sphaceloma manihoticola, causal agent of cassava superelongation disease. Phytopathology 70, 589–593.
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